This is a repository copy of Mega-evolutionary dynamics of the adaptive radiation of birds. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/110927/ Version: Accepted Version Article: Cooney, C.R., Bright, J.A., Capp, E.J.R. et al. (6 more authors) (2017) Mega-evolutionary dynamics of the adaptive radiation of birds. Nature. ISSN 0028-0836 https://doi.org/10.1038/nature21074 Reuse Unless indicated otherwise, fulltext items are protected by copyright with all rights reserved. The copyright exception in section 29 of the Copyright, Designs and Patents Act 1988 allows the making of a single copy solely for the purpose of non-commercial research or private study within the limits of fair dealing. The publisher or other rights-holder may allow further reproduction and re-use of this version - refer to the White Rose Research Online record for this item. Where records identify the publisher as the copyright holder, users can verify any specific terms of use on the publisher’s website. Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by emailing [email protected] including the URL of the record and the reason for the withdrawal request. [email protected] https://eprints.whiterose.ac.uk/ 1 Mega-evolutionary dynamics of the adaptive radiation of birds 2 3 4 Christopher R. Cooney1§, Jen A. Bright1,2,3§, Elliot J. R. Capp1, Angela M. Chira1, Emma 5 C. Hughes1, Christopher J. A. Moody1, Lara O. Nouri1, Zo K. Varley1, Gavin H. 6 Thomas1,4,*. 7 8 9 1Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, 10 UK 11 2School of Geosciences, University of South Florida, Tampa, FL 33620, USA 12 3Center for Virtualization and Applied Spatial Technologies, University of South Florida, 13 Tampa, FL 33620, USA 14 4Bird Group, Department of Life Sciences, The Natural History Museum, Tring, 15 Hertfordshire, UK 16 17 18 § these authors contributed equally 19 * author for correspondence: [email protected] 20 21 22 23 24 25 1 26 The origin and expansion of biological diversity is regulated by both 27 developmental trajectories1,2 and limits on available ecological niches3-7. As 28 lineages diversify an early, often rapid, phase of species and trait proliferation 29 gives way to evolutionary slowdowns as new species pack into ever more 30 densely occupied regions of ecological niche space6,8. Small clades such as 31 Darwin’s finches demonstrate that natural selection is the driving force of 32 adaptive radiations, but how microevolutionary processes scale up to shape the 33 expansion of phenotypic diversity over much longer evolutionary timescales is 34 unclear9. Here we address this problem on a global scale by analysing a novel 35 crowd-sourced dataset of 3D-scanned bill morphology from >2000 species. We 36 find that bill diversity expanded early in extant avian evolutionary history before 37 transitioning to a phase dominated by morphospace packing. However, this early 38 phenotypic diversification is decoupled from temporal variation in evolutionary 39 rate: rates of bill evolution vary among lineages but are comparatively stable 40 through time. We find that rare but major discontinuities in phenotype emerge 41 from rapid increases in rate along single branches, sometimes leading to 42 depauperate clades with unusual bill morphologies. Despite these jumps 43 between groups, the major axes of within-group bill shape evolution are 44 remarkably consistent across birds. We reveal that macroevolutionary processes 45 underlying global-scale adaptive radiations support Darwinian9 and Simpsonian4 46 ideas of microevolution within adaptive zones and accelerated evolution between 47 distinct adaptive peaks. 48 49 The role of adaptive radiations as the source of much of the world’s biological diversity 50 has been widely emphasised10,11. Studies of small clades have provided insights into 51 the role of natural selection as a diversifying force, but cannot illuminate the processes 52 that shape the diversity and discontinuities of radiations over much longer evolutionary 53 timeframes. Indeed, at large taxonomic scales, the diversification of clades11,12 and 54 traits13 shows no evidence of the predicted slowdowns in evolutionary rates, despite 55 there being numerous examples in small clades3,14-16. This apparent paradox is 56 potentially resolved by G. G. Simpson’s model, in which major jumps to new adaptive 57 zones (“quantum evolution”) can occur unpredictably throughout clade history. These 58 jumps give rise to rapid lineage expansion into previously unoccupied niche space as 59 sub-clades continue to radiate within distinct adaptive zones and subzones4. Simpson’s 60 models introduced the concept of ‘mega-evolution’—diversification over large temporal 61 and spatial scales—unifying microevolution with other factors such as ecological 62 opportunity and evolutionary constraints that shape the macroevolutionary trajectories 63 of radiating lineages. However, while phylogenetic studies involving thousands of 64 species have demonstrated heterogeneity in rates of phenotypic evolution13,17, it is 65 unclear whether the processes outlined by Simpson play an important role in large- 66 scale adaptive radiations. This is because previous studies have been unable to 67 specifically assess the macroevolutionary dynamics of ecologically relevant traits. Here 68 we study the evolution of an important ecological trait (bill shape) across an entire Class 2 69 of organisms (birds) to elucidate the processes shaping the accumulation of phenotypic 70 diversity within a global-scale adaptive radiation. 71 72 Our approach is based around a novel data set describing avian bill shape. The avian 73 bill is closely associated with species’ dietary and foraging niches16,18,19 and represents 74 a highly-adaptable ecological trait known to play a key role in classic avian adaptive 75 radiations16,18,20. We took 3D scans of museum study skins comprising >2000 species 76 (>97% of extant genera) representing the full range of bill shape diversity. We 77 landmarked bills (Extended Data Fig. 1) using a bespoke crowd-sourcing website, 78 www.markmybird.org, and quantified the bill shape morphospace of extant birds using 79 Procrustes superimposition and Principal Components Analyses (PCA, see Methods). 80 The first eight PC axes explain >99% of the total variation in bill shape (Fig. 1). PC1 81 (58% of overall shape variation) describes the volumetric aspect ratio from elongated 82 (e.g. sword-billed hummingbird, Ensifera ensifera) to stout bills (e.g. large ground finch, 83 Geospiza magnirostris) and captures the range of shape variation encompassed by 84 standard linear measurements (length, width and depth). Variation in these bill 85 dimensions may relate to fine scale division of the dietary or foraging niche among 86 closely related species, but cannot explain the diversity of shapes observed among 87 extant birds. More complex aspects of shape (42% of total variation) are explained by 88 the remaining PCs (Fig. 1), which retain high phylogenetic signal (Extended Data Table 89 1). Importantly, although these higher shape axes explain a low proportion of shape 90 variance, they capture large differences in ecologically relevant aspects of bill shape. 91 The narrow (long tail) distributions of higher shape axes, compared to the broad 92 distribution of PC1 (Extended Data Fig. 2, Extended Data Table 1), suggest that the 93 majority of species have relatively simple bill shapes and diversify in densely packed 94 regions of bill morphospace. 95 96 We tested an important prediction of Simpson’s model by evaluating how niche 97 expansion and niche packing have contributed to the accumulation of bill shape 98 disparity throughout avian evolutionary history. We estimated multivariate disparity 99 through time using ancestral state estimates derived from rate heterogeneous models of 100 trait evolution (see Methods)13. In 1 million year time slices, we calculated disparity as 101 the sum of the variances21 from the first eight shape axes. We compared observed 102 disparity through time with two null models—constant-rate (Brownian motion) and rate 103 heterogeneous trait evolution—that are unbiased with respect to niche filling processes 104 (see Methods). Relative to these null expectations, we find that the filling of avian bill 105 morphospace through time shows a striking dominance of niche expansion early in 106 avian history, followed by a more recent transition towards niche packing (Fig. 2a-b, 107 Extended Data Fig. 2). Our data includes only extant taxa due to the poor preservation 108 of bills in the avian fossil record22, although we acknowledge that some extinct taxa had 109 bills that may lie outside the range of extant diversity (e.g. Phorusrhacidae, 110 Gastornithidae, Dromornithidae). This can result in underestimates of disparity 111 particularly if these morphologies arise early in clade history22-24. Our analyses are 112 therefore conservative with respect to transitions from bill morphospace expansion to 3 113 filling and consistent with recent studies of avian skeletal material22. The transition in the 114 mode of niche filling is consistent with a process of ever-finer divisions of niche space 115 and would be expected to correspond to slowdowns in rates of bill evolution. However, 116 the switch from niche expansion to niche packing does not map onto temporal trends in 117 the rate of bill shape evolution. Plotting evolutionary rates through time reveals an initial 118 low rate followed by a moderate (two to four-fold) increase that is coincident with the 119 divergence of many non-Passerine orders (Fig. 2c, Extended Data Fig. 3, 4). Thereafter 120 average rates dip and then rise gradually with less than 1.5-fold total variation over ~80 121 million years of evolutionary history, contrasting sharply with >250-fold variation in 122 evolutionary rate among individual lineages (Fig. 3). 123 124 The disjunction between rates of evolution and the accumulation of bill shape disparity 125 suggests that temporal trends in evolutionary rate are not necessarily indicative of the 126 underlying mode of niche filling.